The Vagus Nerve and its Vagaries

SURGICAL ANATOMY AND EMBRYOLOGY

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THE VAGUS NERVE AND ITS VAGARIES Lee John 5kandalakis, MD, FAC5, Philip E. Donahue, MD, and John E. 5kandalakis, MD, PhD, FAC5

"It is true I have not fully seen, but I have fully devined." MARQUIS DE CUSTINE, EMPIRE OF THE CZAR

EMBRYOLOGY The parasympathetic system has a double origin. One is from the brain stem (cranial outflow). The other is from the sacral region (sacral outflow) of the spinal cord (52-53-54). Cranial nerves III, VII, IX, and X originate from the brain stem. Parasympathetics also begin from the sacral region. For all practical purposes, these are, although anatomically interrupted, physiologic continuations of the vagus nerve-its destiny, therefore, being to supply the gastrointestinal tract and in this case the left colon and anorectum. 5pecifically, the vagus nerve originates from the lateral surface of the medulla by the development of several fibers between the origin of the glossopharyngeal nerve above and the bulbar part of the accessory nerve below. 5everal papers by Yoshida et al42-44 in 1988 investigated further distribution of the vagus nerve along the vascular bundles of the greater curvature of the stomach. This contribution provides the experimental basis for extended highly selective vagotomy (EH5V). Donahue et al9 reported that efferent gastric vagal fibers enter the stomach by several routes, and that the neurons supplying the greater curvature could be

From Emory University School of Medicine and Piedmont Hospital, Atlanta, Georgia (LJS, JES); Cook County Hospital and the University of Illinois at Chicago, Chicago, Illinois (PED); and The Medical College of Georgia, Augusta, Georgia (JES)

SURGICAL CLINICS OF NORTH AMERICA VOLUME 73 • NUMBER 4 • AUGUST 1993

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defined as a subset of the neurons that constitute the dorsal motor nucleus of the vagus nerve. As part of the same project, Yoshida et a141 demonstrated that the neurovascular bundles along the greater curvature of the stomach contain preganglionic efferent vagus nerve fibers by experimenting on rats and ferrets. These authors stated that the neurovascular bundles along the greater curvature contain efferent vagal preganglionic fibers with their cells' origin localized in the dorsal motor nucleus of the vagus at the vicinity of the obex. They described preganglionic nerves originating in the right and left sides of the dorsal motor nucleus of the vagus nerve. They concluded that proximal gastric vagotomy limited to dissection at the gastroesophageal junction and the lesser curvature does not include some of the preganglionic fibers that innervate the parietal cell mass. In an elegant series of experiments, partially based on those previously described, Berthoud and Powley'" b were able to verify antegrade transport of a neurotracing compound (Dil) from the dorsal motor nucleus of the vagus to the nerves of the greater curvature. The same authors stimulated the nerves of the greater curvature following division of other gastric vagal fibers and found definite evidence of acid secretion. Gastric Vagus Nerves

Although 80% of vagus neurons are afferent in nature, surgeons generally have focused their attention upon efferent nerve functions. Foley and DuBois 12 reported, from experiments with cats, that sensory vagal fibers range from 65% to 80%. This conclusion was based on the percentage of central nervous system neurons that showed degenerative changes after division of the peripheral nerve. Because retrograde degeneration would affect only a certain number of cells, the answer was relatively easy to deduce. 4 ANATOMY

The left and right vagus nerves descend parallel to the esophagus and form the esophageal vagal plexus between the level of the tracheal bifurcation and the level of the diaphragm. From this plexus, two vagal trunks, anterior and posterior, form and pass through the esophageal hiatus of the diaphragm. Each trunk subsequently separates into two divisions (Fig. 1). From the anterior trunk, the hepatic division passes to the right in the lesser omentum, branching before it enters the liver. One branch turns downward to reach the pylorus and sometimes the first part of the duodenum. The second division, the anterior gastric, descends along the lesser curvature of the stomach, giving branches to the anterior gastric wall. From the posterior trunk arises the celiac division, which passes to the celiac plexus, and the posterior gastric division, which supplies branches to the posterior gastric wall.

THE VAGUS NERVE AND ITS VAGARIES

Right vagus nerve

Left vagus nerve

.~~ Posterior vagal trunk - -

771

----+';o;;f',','J !'.:'~---.

Esophageal plexus

Anterior vagal trunk

••

Figure 1. The terminology of vagal structures of the thorax and abdomen. In this example, two vagal trunks pass through the hiatus to enter the abdomen. 1 = hepatic division; 2 = anterior gastric division; 3 = celiac division; 4 = posterior gastric division. (From Skandalakis JE, Rowe JS, Gray SW, et al: Identification of vagal structures at the esophageal hiatus. Surgery 75:233-237,1974; with permission.)

IDENTIFICATION OF VAGAL STRUCTURES AT THE HIATUS

To the surgeon planning a truncal vagotomy, the pattern of the vagus nerves at the esophageal hiatus is important. The basic configuration and variations are well knownY' 16. 18 The thoracic pattern, however, is not visible to the abdominal surgeon, who must proceed on the basis of the structures that can be seen. In our study of vagal structures in 100 cadavers/7 we found the following (Table 1): (1) two vagal structures only in 88% (see Fig. 1). These will be the anterior and posterior vagal trunks, which have not yet split to form the four typical divisions. Both trunks are usually to the right of the midline of the esophagus. The posterior trunk lies closer to the aorta than to the esophagus (Fig. 2); (2) four vagal structures in 7% (Fig. 3). These will be the four divisions of the vagal trunks. Division has occurred above the diaphragm; (3) more than four vagal structures in 5%. These may be divisions and branches of divisions (see Fig. 3) (the anterior and posterior trunks lie entirely within the thorax), and elements

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Table 1. NUMBER OF VAGAL STRUCTURES PASSING THROUGH THE ESOPHAGEAL HIATUS No. of Hiatal Vagal Structures

No. of Specimens

Terminology of Hiatal Vagal Structures

2 4

88 7

>4 >4

2 3

Vagal trunks Divisions Divisions and/or branches of divisions Elements of the esophageal plexus

Total

100

From Skandalakis JE, Rowe JS Jr, Gray SW, Androulakis JA: Identification of vagal structures at the esophageal hiatus. Surgery 75:233-237,1974; with permission.

of the esophageal vagal plexus (see Fig. 3) (the anterior and posterior trunks lie entirely within the abdomen). Nerve structures at the hiatus, in addition to the usual two, have sometimes been called laccessory."40 This term is incorrect. True accessory nerves would have to originate from the esophageal plexus and descend without making further connection with the normal vagal trunks. In our experience, all such parallel descending fibers rejoin the normal trunks below the diaphragm, which shows them to be part of the esophageal plexus. Branches of the divisions, especially those of the posterior gastric division, are inconstant. Where they originate above the diaphragm, there may be several branches descending through the hiatus. Indeed, among jackson's 50 specimens/ 8 there were only two in which the posterior gastric division originated as a single bundle. Such branches of divisions are not accessory. 80 1 8

~=k RIGHT

I

LEFT

761 12 •

I •

Post. vagal trunk

~,a 1

Figure 2. The relation of the anterior and posterior vagal trunks to the aorta and the esophagus. As reflected in 88 specimens, the trunks are usually to the right of the midline; the anterior trunks are closer to the esophagus than are the posterior trunks. (From Skandalakis JE, Rowe JS, Gray SW, et al: Identification of vagal structures at the esophageal hiatus. Surgery 75:233-237,1974; with permission.)

A

B

c

Post vagal trunk--

Diaphragm

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Esopho(,leal plexus

Figure 3. Where four or more vagal structures emerge through the hiatus, they may be: A, Divisions that have separated just above the diaphragm; B, divisions and their branches that arise above the diaphragm; or C, elements of the esophageal plexus that extend below the diaphragm. The vagal trunks are entirely within the abdomen. 1 = hepatic division; 2 = anterior gastric division; 3 = celiac division; 4 = posterior gastric division. (From Skandalakis JE, Rowe JS, Gray SW, et al: Identification of vagal structures at the esophageal hiatus. Surgery 75:233-237, 1974; with permission.) '-l

~

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DISTRIBUTION OF THE VAGAL NERVES TO THE STOMACH Anterior Gastric Division

Among 100 specimens we have dissected,35 the separation of the anterior gastric and hepatic divisions occasionally occurred above the diaphragm, but usually lay on the abdominal esophagus or the cardia. In 96 of our 100 specimens, a major branch of the anterior gastric division formed the principal anterior nerve of the lesser curvature (anterior nerve of Latarjet). It usually lay from 0.5 to 1.0 cm from the lesser curvature. In one of the specimens it lay beneath the serosa of the gastric wall. This nerve can be traced distally to about the level of the incisura in most subjects, but in many it reaches the pylorus, and in a few it is visible as far as the first part of the duodenum (Fig. 4 and Table 2). Legros and Griffith23 have shown that vagal branches that are subserosal at the surface may penetrate the muscularis and continue downward to the antrum by the submucosal (Meissner's) plexus. From 2 to 12 branches pass from the principal nerve to the stomach wall. The average in our subjects was six. In two of our subjects, the anterior nerve of Latarjet was duplicated; each nerve supplied its own branches to the stomach wall (see Fig. 4). Loeweneck24 has called the longer of these nerves the antral nerve. In some subjects there is no true nerve of Latarjet; a fan of gastric branches arises from the anterior vagal trunk above the origin of the hepatic division, and one or more long branches below this origin descend to supply the antrum (see Fig. 4). Even where a definite nerve of Latarjet is present, there are usually some, and often many, branches to the gastric cardia and fundus that arise from the anterior trunk proximal to the origin of the hepatic division (see Fig. 4). Although we have often seen the nerve of Latarjet branch in the "crow's foot" formation, this pattern is far from constant, being equivocal in some cases and absent in many. The term "crow's foot" was originally applied to the termination of the left gastric artery at the same location by Payne. 31 Hepatic Division

The hepatic division of the anterior vagal trunk usually separates from the anterior gastric division at the level of the abdominal esophagus (see Fig. 4). It lies between the leaflets of the avascular portion of the gastrohepatic ligament. It is frequently found in multiple and usually closely parallel branches (see Fig. 4 and Table 3). Posterior Gastric Division

In most subjects, the posterior gastric division forms the principal posterior nerve of the lesser curvature (posterior nerve of Latarjet). As a

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775

( B

A

E

c

D

G F Figure 4. The anterior views of several selected specimens. A, Innervation of the pylorus by the anterior gastric division and the pyloric branch of the hepatic division. B, The double nerve of Latarjet. C, No typical nerve of Latarjet is present. D, The gastric branches originate from the hepatic division. E, Multiple hepatic divisions are shown. F, Low origin of the hepatic division. G, The pyloric branch arises from the anterior gastric division. (From Skandalakis JE, Gray SW, Soria RE, et al: Distribution of the vagus nerve to the stomach. Am Surg 46:130-139,1980; with permission.)

rule, the posterior nerve appears to terminate slightly higher on the lesser curvature and possesses fewer gastric branches than does the anterior nerve. In no case has a posterior nerve been observed to reach the duodenum.

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Table 2. VISIBLE DISTAL EXTENT OF THE ANTERIOR AND POSTERIOR GASTRIC DIVISIONS OF THE VAGUS Termination Above the incisura At the incisura At or above the incisura Just below the incisura At the pylorus At the first part of the duodenum

No. of Anterior Divisions

No. of Posterior Divisions

6 17

21 4 71 1 3

62 6 3 6

100

Totals

o

100

From Skandalakis JE, Gray SW, Soria RE, et al: Distribution of the vagus nerve to the stomach. Am Surg 46:130-139,1980; with permission.

In a number of specimens, the gastric branches of the posterior nerve of Latarjet fell into a superior and inferior group. The superior branches arose from the posterior vagal trunk just below or even above the diaphragm. The inferior branches arose from the descending posterior nerve of Latarjet and supplied only the lower body and the antrum. Between these two groups of branches, the lesser curvature had no grossly visible nerve supply. In many of our specimens, the most superior gastric branch, the "criminal nerve" of Grassi,t4 arose at or above the origin of the celiac division (Fig. 5). Usually no single branch seemed worthy of this dramatic term. In 18 of our 100 specimens, a true posterior nerve of Latarjet was absent; branches arising from the celiac division turned back toward the lesser curvature, and one or more long branches descended to innervate the antrum (see Fig. 5).

Table 3. VARIATIONS IN NUMBER AND POSITION OF ELEMENTS OF THE HEPATIC DIVISION OF THE VAGUS Pattern Single In normal position From distal lesser curvature Contributions from both vagal trunks Bifurcated: In normal position Double Both in normal position One from middle of lesser curvature Triple All in normal position One from middle of lesser curvature Quadruple: All in normal position Total

No.

71 1 5 3 2 2 3 1

12

100

From Skandalakis JE, Gray SW, Soria RE, et al: Distribution of the vagus nerve to the stomach. Am Surg 46:130-139, 1980; with permission.

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c

B

~f

1~

D

E

F

Figure 5. Patterns of the posterior gastric and celiac divisions of the posterior vagal trunks. (From Skandalakis JE, Gray SW, Soria RE, et al: Distribution of the vagus nerve to the stomach. Am Surg 46:130-139, 1980; with permission.)

Celiac Division

The celiac division is the largest of the four vagal divisions. It lies in the gastropancreatic peritoneal fold. In all cases it was single and led directly to the celiac plexus. This division may follow the left gastric artery or the right crus of the diaphragm or may take an intermediate position in the triangle bounded by the artery, the crus, and the right margin of the stomach. Vagal fibers connect the stomach with the brainstem as they terminate in the gastric mesenteric plexus. The precise mode of nerve-gut interaction; however, is elusive and cannot be addressed here. SYMPATHETIC INNERVATION

The splanchnic nerves contain afferent and efferent fibers, and together with celiac ganglia form the sympathetic innervation of the stomach and the duodenum. Regarding efferent fibers, preganglionic fibers from Ts to TlO form the splanchnic nerves, which terminate in the celiac ganglia. Postganglionic fibers from the celiac ganglia reach the stomach and duodenum via their blood supply.

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Afferent fibers follow the same pathway. Therefore, the sympathetic nervous system is the connection of the stomach to the spinal cord via sympathetic and dorsal root ganglia, by efferent fibers that start in the ganglia and end in the gastric wall as target cells, and by afferent fibers that most likely originate in the gastric wall or in the dorsal root ganglia. THE VAGARIES OF THE VAGUS: APPLICATIONS

The student of the vagus nerve, the surgeon performing proximal gastric vagotomy, wonders of course about the correct anatomy of the vagus and the completeness of the vagotomy, because he or she accepts only the orthodox anatomy and the accepted technique of proximal gastric vagotomy by "parasympathetic denervation" of the proximal two thirds of the stomach, preserving the antral and pyloric innervation as well as the hepatic and celiac divisions. This "denervation" is accomplished by sectioning gastric branches of the anterior and posterior nerves of Latarjet from the gastroesophageal junction (abdominal esophagus) to the crow's foot. Highly Selective Vagotomy

The first highly selective vagotomy (HSV) was performed in 1967 by Holle and Hart, who included a type of pyloric reconstruction in most cases. Johnston and Wilkinson19 in 1969 reported that selective vagotomy without a drainage procedure was an effective operation. Later, these authors reported a very low mortality: 17 deaths in 5539 cases.20 The operation, as they performed it, would remain essentially unchanged for almost 20 years. For denervation of the acid-secreting corpus, Donahue6 advised extended proximal vagotomy based upon clinical intraoperative testing for completeness of vagotomy with Congo red dye, supplemented by experimental research9 (Fig. 6). He described the following steps for EHSV: (1) 5 to 6 cm periesophageal dissection of the distal esophagus; (2) baring from the cardia to the antrum the lesser gastric curvature; (3) division of the gastropancreatic fold from the lesser curvature to the first short gastric vessel; (4) division of the right and left gastroepiploic nerves of the greater curvature; and (5) dissection of the crow's foot including heel and "instep." Note, too, the following considerations in the procedure. (1) The peritoneal fold is at the posterior wall of the omental bursa from the cardiac and of the lesser curvature to the greater curvature where the short gastrics are located. Responsible for this fold is the left gastric artery, but occasionally there are folds from the stomach to the pancreas that are not related to the left gastric artery. Grant and Basmajian13 speak about a left gastropancreatic fold as a mesentery of the left gastric artery from the esophageal hiatus to the

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Figure 6. The seven areas of vagotomy. Preganglionic efferent vagus nerves reach the parietal cell mass in seven areas. Area 1 is the periesophageal region; area 2 is the lesser curve of the stomach; area 3 is the crow's foot area; area 4 is represented by the dotted line, as the gastropancreatic fold is not visible anteriorly; area 5 is the region of short gastric vessels; area 6 is the left gastroepiploic pedicle; and area 7 is the right gastroepiploic pedicle. Areas 3, 4, 6, and 7 are divided routinely during extended highly selective vagotomy. Area 5 is preserved because the nerves at this site cannot be divided without sacrificing essential blood supply to the proximal part of the stomach. (From Donahue PE, Richter HM, Liu KJM, et al: Experimental basis and clinical application of extended highly selective vagotomy for duodenal ulcer. Surg Gynecol Obstet 176:40, 1993; with permission of Surgery, Gynecology and Obstetrics.)

lesser curvature. Is there any right gastropancreatic fold? What about the superior and inferior gastropancreatic folds of Romanes raised by the left gastric and hepatic arteries, respectively? Is the superior fold the one with which we are interested? Most likely so. Therefore, perhaps the right fold is related to the hepatic artery and the left one to the left gastric, but for the completion of the third step of Donahue's technique the tissue or plica or fold between the lesser curvature and the first short gastric artery should be divided; this is the fold of tissue containing the posterior gastric artery (a branch of the splenic artery that we see in every case of EHSV). (2) The right and left gastroepiploic nerves are traveling with the gastroepiploic vessels.

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(3) The instep of the crow's foot, according to Donahue, is the tissue between the terminal branches of the anterior and posterior nerves of Latarjet.

The "Acid Antrum" and the Parietal Cell Mass Extension

In 1961 Lowicki and Littlefield25 experimentally defined the dimensions of the gastric antrum. In 1965, Moe, Klopper, and Nyhus27 demonstrated the functional anatomy of the canine gastric antrum. Griffith,15 one of the original investigators of cell mass extension distally utilizing Congo red pH, presented an excellent chapter about the anatomy of the stomach and duodenum, the anatomic variations of the distal extension of the antrum toward the gastroduodenal junction, and the variable lengths of the nerve of Latarjet. Griffith stated that in some patients the parietal cell mass extended to within 2 cm of the pylorus. Also, he presented findings of several authors such as McCrea,26 Skandalakis et al/5- 37 and Latarjet,22 describing the length of the anterior nerve of Latarjet, which may be short (8.5 cm from the pylorus) or traveling down to the first part of the duodenum. Griffith agrees with Poppen et aP3 that there is no connection between the distal extent of the parietal cell mass extension and the distal extent of the anterior nerve of Latarjet. Popiela and Turczynowskp2 reported, however, that the corpus-antrum border is located by the last branch of the anterior nerve of Latarjet and is occasionally longer than the anterior in the same patient, and also that an acid secretion is caused by the nerves entering the greater curvature of the stomach. Both groups, the Cracow and the Chicago, differ as to the end results of the Congo red test and its clinical applications for the treatment of duodenal ulcer. The Chicago group believes, however, that the size of antrum does not make any difference for the use of proximal gastric vagotomy; the Cracow group, which utilized Congo red testing without preliminary alkalinization of the gastric mucosa (T. Popiela, personal communication), may have been misled by acid secreted in other portions of the stomach. If acid from the proximal stomach were present in the gastric antrum at the time of Congo red testing, but without alkalinization, then the observer would see a rapid red-black color change (indicative of the presence of acid) in the antrum. When we say "acid antrum" we mean a downward distal extension of the parietal cell mass in the pyloric area. Investigators disagree about the location of the corpus-antrum line, from 1 to 8.5 cm from the pylorus. Naik et aF8 (the Johnston group) found an "acid antrum" in 16% of the cases, reporting that the border of the parietal cells exceeded the anatomic border by more than 1 cm. Further, Derbyshire et al5 reported that parietal cells extended to the distal part of pylorus in 35%, with the possibility of vagal innervation up to 55%. The same authors stated that the anterior vagal trunk terminated on the posterior antral surface in 25%, and the posterior trunk reached the anterior surface in 20%.

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Proximal gastric vagotomy as a procedure of choice for the treatment of duodenal ulcer is a good procedure for the following reasons: (1) minimal operating room mortality; (2) minimal operating room anatomic complications; (3) minimal late complications; (4) acceptable reduction of gastric acidity; and (5) acceptable recurrence rates. Valen et aP8 stated, however, that several problems remain to be solved after they reviewed 483 patients for 3 to 14 years who underwent proximal gastric vagotomy for peptic ulcer disease. Four of their patients suffered necrosis of the lesser curvature, with one death, and their overall recurrence rate was approximately 13%. Kellil reported 12% recurrence. In another publication, Valen and Halvorsen39 advised that reperitonealization of the lesser curvature was without benefit. We wonder, however, why? Braghetto et aP do not advocate EHSV to reduce gastric acid postoperatively. However, in a reply, Donahue and Nyhus7 disagree. Perhaps in the near future, if Donahue et apo and Rosati et aP4 are right, gastric acidity and recurrence will be reduced in such a way that the extended proximal gastric vagotomy will be the ideal procedure, with open or laparoscopic technique. In their recent report, Donahue et al8 describe an overall recurrence rate of less than 2.0%, with an average 5-year follow-up for patients with complications of duodenal ulcer treated by EHSV. According to CuschierV the following procedures may be performed by laparoscopy: (1) thoracoscopic truncal vagotomy and pyloric stretch; (2) laparoscopic truncal vagotomy and pyloric stretch; (3) laparoscopic highly selective vagotomy; (4) laparoscopic posterior truncal vagotomy and anterior seromyotomy; and (5) anterior highly selective vagotomy and posterior truncal vagotomy. This is an anatomic article. We make no attempt to "muddy up" the water, which is already confusing. We need more physiologic studies and more randomized studies, and then the student of the vagus nerve and its vagaries will begin to criticize the several procedures. Six years ago, Nyhus29 discussed the problems. It is up to us to decide what we believe. In the armamentarium of the surgeon, the laparoscopic vagotomy is very promising. It is too early to express definite opinions, and by all means we do not wish to make such statements as Gross and Paget made in the past. Once Samuel D. Gross, in A System of Surgery, stated," ... can the thyroid gland, when in a state of enlargement, be removed with a reasonable hope of saving the patient? Experience emphatically answers no . . . . No honest and sensible surgeon, it seems to me, would ever engage to it."17 Eight years later, in 1874, Theodor Kocher at the age of 31, extirpated successfully a thyroid gland. Another patriarch of surgery, Stephen Paget, wrote, "Surgery of the heart has probably reached the limits set by Nature to all surgery: no new methods and no new discovery can overcome the natural difficulties that attend a wound of the heart. It is true that heart suture has been vaguely proposed as a possible procedure, and that it has been done on

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animals, but I cannot find that it has ever been attempted in practice."30 One year later Rehn in Frankfurt reported the successful closure of a stab wound in the right ventricle of a young man who completely recovered. SUMMARY

Without any further comments we advise the surgeon performing open or laparoscopic vagotomy to know the anatomy and the vagaries of the vagus nerve. In view of the demonstration that the nerves of the greater curvature, identified as a concern in achieving a "complete" PGV, are projected from up to 20% of the nerve cell bodies of the dorsal motor nucleus of the vagus nerve in the brain stem, we believe it is appropriate to adopt the technique of EHSV as a means of avoiding the high recurrence rates reported with conventional highly selective vagotomy or proximal gastric vagotomy. When pyloric stenosis or outlet obstruction is present, anterior hemipylorectomy provides a solution. If surgeons adopt a laparoscopic approach to EHSV, they must be cognizant of all sites of preganglionic innervation, and (ideally) attempt to verify the "completeness" of vagotomy by Congo red testing. We look forward, also, to the work of Andrus and Schneider, who are evaluating alternative methods of achieving complete vagotomy. References a. Berthoud HR, Powley TL: Vagal afferent innervation of the rat fundic stomach: Morphological characterization of the gastric tension receptor. J Comp Neurol319:261-276, 1992 b. Berthoud HR, Fox EA, Powley TL: Abdominal pathways and central origin of rat vagal fibers that stimulate gastric acid. Gastroenterology 100:627-637, 1991 1. Braghetto I, Csendes A, Lazo M, et al: A prospective, randomized study comparing highly selective vagotomy and extended highly selective vagotomy in patients with duodenal ulcer. Am J Surg 155:443, 1988 2. Bruckner WL: Gastric secretion and motility after highly selective sympathectomy. In Holle F, Andersson S (eds): Vagotomy. New York, Springer-Verlag, 1974, p 89 3. Cuschieri A: Laparoscopic vagotomy: Gimmick or reality? Surg Clin North Am 72:357367,1992 4. Debas HT: Physiology of gastric secretion and emptying. In Miller TA (ed): Physiologic Basis of Modem Surgical Care. St. Louis, CV Mosby, 1988, p 280 5. Derbyshire SA, Lagopoulos M, Lee T, et al: Distribution of the vagus nerve to the human pyloric antrum and possible surgical implications. Clinical Anatomy 3:25-31, 1990 6. Donahue PE: Extended proximal vagotomy with drainage. In Nyhus LM, Baker RJ (eds): Mastery of Surgery. Boston, Little, Brown, 1992, p 686 7. Donahue PE, Nyhus LM: To the Editor. Am J Surg 158:79-80, 1989 8. Donahue PE, Richter HM, Liu KJ, et al: Experimental basis and clinical application of extended highly selective vagotomy. Surg Gynecol Obstet 176:39-48, 1993 9. Donahue PE, Yoshida J, Polley EH, et al: Preganglionic vagus nerve fibers also enter the greater curvature of the stomach in rats and ferrets. Gastroenterology 94:1292-1299, 1988 10. Donahue PE, Bombeck T, Condon RE, Nyhus LM: Proximal gastric vagotomy versus selective vagotomy with antrectomy. Surgery 96:585-590,1984 11. Dragstedt LR, Fournier HJ, Woodward ER, et al: Transabdominal gastric vagotomy: A study of the anatomy and surgery of the vagus nerves at the lower portion of the esophagus. Surg Gynecol Obstet 85:461, 1947

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